A comparative study of eleven protein systems in tamarins, genus Saguinus (Platyrrhini, Callitrichinae)

Carla Meireles Iracilda Sampaio Horacio Schneider Stephen F. Ferrari Adelmar F. Coimbra-Filho Alcides Pissinatti Maria P.C. Schneider

Abstracts

The genetic variability of six tamarin taxa, genus Saguinus, was analyzed comparatively using protein data from eleven systems coded by 15 loci. S. fuscicollis weddelli and S. midas midas were the most polymorphic taxa, and S. bicolor the least. The results of the phylogenetic analyses (UPGMA and neighbor-joining) and the genetic distances between taxa were generally consistent with their geographic and probable phylogenetic relationships. Analyses of the S. bicolor and S. midas populations suggested that they represent no more than three subspecies of a single species, S. midas, with the bicolor forms belonging to a single subspecies, S. midas bicolor. If supported by additional studies, this would have important implications for the conservation of the bicolor form, which is endangered with extinction. The genetic similarity of S. fuscicollis and S. mystax was also consistent with their geographical and morphological proximity, although more data from a larger number of taxa will be required before the taxonomic relationships within the genus can be defined.


A variabilidade genética de seis taxa de tamarins, gênero Saguinus, foi analisada comparativamente usando-se dados protéicos de onze sistemas codificados por quinze loci. S. fuscicollis weddelli e S. midas midas foram os taxa mais polimórficos, enquanto S. bicolor foi o menos. Os resultados da análise filogenética (UPGMA e neighbor-joining) e as distâncias genéticas entre os taxa foram em geral consistentes com suas relações geográficas e filogenéticas. As análises das populações de S. bicolor e S. midas indicaram que eles podem representar não mais do que três subespécies de uma única espécie, S. midas, com as formas de bicolor pertencendo a uma única subespécie, S. midas bicolor. Se apoiado por estudos adicionais, este fato teria implicações importantes para a conservação da forma de bicolor, que está em perigo de extinção. A similaridade genética de S. fuscicollis e S. mystax foi também consistente com sua proximidade geográfica e morfológica, embora mais dados sobre um número maior de taxa seriam necessários antes de se definirem as relações taxonômicas dentro do gênero.


A comparative study of eleven protein systems in tamarins, genus Saguinus (Platyrrhini, Callitrichinae)

Carla Meireles 1 , Iracilda Sampaio 1 , Horacio Schneider 1 , Stephen F. Ferrari 1 , Adelmar F. Coimbra-Filho 2 , Alcides Pissinatti 2 and Maria P.C. Schneider 1

1Departamento de Genética, Centro de Ciências Biológicas, Universidade Federal do Pará,

Campus Universitário do Guamá, Caixa Postal 8607, 66075-900 Belém, PA, Brasil.

Tel: (091) 211-1627, Fax: (091) 211-1568. Send correspondence to M.P.C.S.

2Centro de Primatologia do Rio de Janeiro, CPRJ FEEMA, Rio de Janeiro, Brasil.

ABSTRACT

The genetic variability of six tamarin taxa, genus Saguinus, was analyzed comparatively using protein data from eleven systems coded by 15 loci. S. fuscicollis weddelli and S. midas midas were the most polymorphic taxa, and S. bicolor the least. The results of the phylogenetic analyses (UPGMA and neighbor-joining) and the genetic distances between taxa were generally consistent with their geographic and probable phylogenetic relationships. Analyses of the S. bicolor and S. midas populations suggested that they represent no more than three subspecies of a single species, S. midas, with the bicolor forms belonging to a single subspecies, S. midas bicolor. If supported by additional studies, this would have important implications for the conservation of the bicolor form, which is endangered with extinction. The genetic similarity of S. fuscicollis and S. mystax was also consistent with their geographical and morphological proximity, although more data from a larger number of taxa will be required before the taxonomic relationships within the genus can be defined.

INTRODUCTION

The tamarins, Saguinus spp., are small-bodied platyrrhine monkeys distributed in Amazonia and northwestern Colombia/eastern Panama. Saguinus is the most diverse of New World monkey genera, with 33 currently recognized taxa, including at least 10 species (Hershkovitz, 1977). The classic reviews of Hershkovitz (1977, 1979, 1982) divide the tamarins into three "sections" based on the characteristics of the facial pelage (hairy face, mottled face and bare face), and six species groups (Table I). Natori and Hanihara (1992), Ferrari (1993) and Rylands et al. (1993) have all proposed minor alterations to these groupings (Table I).

Despite being the most diverse of platyrrhine genera, Saguinus has fewer species than either Callicebus (Hershkovitz, 1990) or Callithrix (de Vivo, 1991; Mittermeier et al., 1992), even if the suggested modifications of Mittermeier et al. (1988), Thorington (1988) and Coimbra-Filho (1990) are incorporated. In addition to the 10 species identified by Hershkovitz (Table I), Mittermeier et al. (1988) recognize the geoffroyi form as a true species (see also Hanihara and Natori, 1987), and Thorington (1988) gives species status to tripartitus. Coimbra-Filho (1990) has also supported the more traditional classification of the bleached forms of the saddle-back tamarins (acrensis, crandalli and melanoleucus) as members of Saguinus melanoleucus.

Table I - Taxonomy of the genus Saguinus, according to Hershkovitz (1977, 1979, 1982).

(1) Ferrari (1993) places this species in the S. mystax group, and puts the S. fuscicollis forms in a separate group.

(2) Natori and Hanihara (1992) and Rylands et al. (1993) place S. bicolor in the S. midas group, to which Ferrari (1993) adds S. inustus.

The most recent overview of Saguinus taxonomy (Rylands et al., 1993) recognizes 12 species, including Saguinus geoffroyi and Saguinus tripartitus, but excluding S. melanoleucus, although neither this arrangement, nor that of Mittermeier et al. (1988), was based on the collection or analysis of quantitative data.

In the light of recent trends (e.g. Hershkovitz, 1990; de Vivo, 1991), Mittermeier et al. (1992) support the need for a detailed taxonomic revision of the genus Saguinus. The analysis of genetic variables has been an important element lacking, to a greater or lesser extent, in the most traditional studies of callitrichine subgeneric systematics. This is at least partly due to the relative lack of genetic data, at least until recently (Nagai et al. (1986); Melo et al. (1992); Dantas (1994); Nagamachi (1995), and Meireles, C., Sampaio, I., Schneider, H., Ferrari, S.F., Coimbra-Filho, A.F., Pissinatti, A. and Schneider, M.P.C., unpublished results).

MATERIAL AND METHODS

Eleven protein systems were analyzed using 322 blood samples of six Saguinus taxa (Table II): Saguinus mystax (SMY), Saguinus bicolor bicolor (SBB), Saguinus bicolor martinsi (SBM), Saguinus fuscicollis weddelli (SFW), Saguinus midas midas (SMM) and Saguinus midas niger (SMN). Fifty blood samples of Alouatta belzebul belzebul (ABB) (family Atelidae sensu Schneider et al., 1993) were also analyzed and used as an outgroup (Table II).

Table II - Species and subspecies of tamarins analyzed, collecting sites and sample sizes.

INPA - Instituto de Pesquisas da Amazônia.

States of Brazil: RO - Rondônia; AP - Amapá; AM - Amazonas; PA - Pará.

For the collection of blood samples, monkeys were anesthetized with Ketalar (ketamine chloride, Park Davis) at a dose equivalent to 10 mg/kg body weight. Samples were processed following Sampaio and Schneider (1986): centrifuged at 3,000 rpm for 10 min at room temperature, red cells were isolated and glycerolized, and both plasma and cells were stored at -20oC before being analyzed.

Horizontal electrophoresis was carried out in the following media: 0.8% agarose, 0.8% agarose 2% starch and 11% starch gels. Two types of starch were used: potato starch (Sigma) and corn starch (Penetrose 30). The following 11 protein systems coded by 15 loci were investigated:

- lactate dehydrogenase (LDHA, LDHB, E.C. 1.1.1.27);

- malate dehydrogenase 1 (MDH1, E.C. 1.1.1.37);

- isocitrate dehydrogenase 1 (IDH1, E.C. 1.1.1.42);

- phosphogluconate dehydrogenase (PGD, E.C. 1.1.1.44);

- superoxide dismutase 1 (SOD1, E.C. 1.15.1.1);

- phosphoglucomutase 1 (PGM1, E.C. 2.7.5.1);

- esterases (ESD, ES1, ES2, E.C. 3.1.1.1);

- acid phosphatase 1 (ACP1, E.C. 3.1.3.2);

- carbonic anhydrase 2 (CA2, E.C. 4.2.1.1);

- hemoglobin (HBA, HBB) and

- albumin (ALB).

Electrophoretic conditions and staining procedures followed Harris and Hopkinson (1976). The medium, time of migration and the difference of potential used for each protein system are shown in Table III, and the buffers in Table IV. Gene frequencies were estimated by maximum likelihood using Reed and Schull’s (1968) MAXLIK program, and genetic variability (average heterozygosity, proportion of polymorphic loci and mean number of alleles per locus) was calculated according to Nei (1987). The matrix of genetic distances (unbiased minimum distance) and identities (unbiased genetic identity) were calculated according to Nei’s (1978) method. The trees were estimated by the neighbor-joining method (Saitou and Nei, 1987). All estimates were carried out using the DISPAN program (Kumar et al., 1993).

Table III - The 11 protein systems investigated, with the electro- phoretic conditions employed in the analysis.

Table IV - Buffers used for the electrophoretic analysis.

PC = pH 5.9, 245 mM monobasic sodium phosphate, 150 mM citric acid; PCE = pH 6.9, 110 mM monobasic sodium phosphate, 75 mM trissodium citrate, 2.5 mM EDTA; TEMM = pH 7.4, 100 mM Tris, 100 mM maleic anhydride, 10 mM EDTA, 10 mM magnesium chloride; TEB1 = pH 8.6, 180 mM Tris, 100 mM boric acid, 4 mM EDTA; TEB2 = pH 6.9, 30 mM Tris, 300 mM boric acid, 4.3 mM EDTA.

RESULTS

The nomenclature of the electrophoretic phenotypes in this study was established by means of intra- and inter-populational comparisons of the observed patterns, using the notation for A. belzebul (Schneider, 1988) as standard. The new phenotypes were numbered sequentially in ascending order starting from the most anodal to the most cathodal, and were nominated in accordance with Shows et al. (1979).

Nine polymorphic loci (MDH1, IDH1, PGD, SOD1, PGM1, ESD, ES2, CA2 and ALB) were observed in the six populations of Saguinus, while six loci were monomorphic: LDHA, LDHB, ES1, ACP1, HBA and HBB. Allelic frequencies are presented in Table V.

Table V - Gene frequencies of 15 loci analyzed in seven populations of tamarins.

Populations identified in Table II.

Genetic variability, measured using average heterozygosity, proportion of polymorphic loci and mean number of alleles per locus is shown in Table VI. S. midas midas and S. fuscicollis weddelli were the most varied of the tamarins, while the two bicolor subspecies exhibited the lowest variation.

Table VI - Average heterozygosity, proportion of polymorphic loci and mean number of alleles per locus in the seven populations of primates.

N = Number of animals; L = number of loci; H(%) = average heterozygosity; SD(%) = standard deviation; P(%) = proportion of polymorphic loci; A = mean number of alleles per locus.

Genetic distances (D) in Saguinus species varied from 0.1% (between the two subspecies from Saguinus bicolor, see Table VII) to 20% (between S. b. bicolor and S. mystax). The highest distance value observed between a tamarin (S. b. bicolor) and the atelid outgroup (A. belzebul) was 71% and the lowest 63% (S. f. weddelli x A. belzebul). Figures 1 (UPGMA) and 2 (neighbor-joining) show the phylogenetic trees for the seven populations obtained from the protein data.

Table VII - Matrix of genetic distance (below) and genetic identity (above) between the Saguinus and Alouatta populations.

Figure 1 - UPGMA tree showing the relationships among the Saguinus species and Alouatta belzebul. Numbers at the nodes are bootstrap values from 2000 replicates.

Figure 2 - Neighbor-joining tree showing the relationships among the Saguinus species and Alouatta belzebul. Numbers at the nodes are bootstrap values from 2000 replicates.

DISCUSSION

The frequencies of some alleles differed significantly between subspecies, species, genera, and families, while others were found exclusively in either a single species or species group. Thus, these alelles are important biochemical markers for the analysis of callitrichine phylogeny, and can be divided into four categories:

(i) markers present in a single subspecies:

S. midas midas - PGD7 (4%) and SOD14 (12%);

S. midas niger - PGD3 (8%), PGD6 (9%) and ES24 (3%);

S. b. bicolor - IDH13 (14%);

S. b. martinsi - PGD5 (13%);

(ii) markers present in a single species:

S. mystax - MDH11 (2%) and PGM13 (11%);

S. fuscicollis - CA23 (53%), CA24 (47%) and ALB1 (6%);

S. midas - ESD1 (7%), and CA27 (57%);

S. bicolor - ES11 (100%);

(iii) markers that differentiate species groups:

Hairy-face tamarin group - ES12;

Bare-face tamarin group - ES11;

(iv) markers present in a single genus:

Saguinus (Callitrichinae) - PGM12, ACP11, HBA1, HBB1 and ALB2;

Alouatta (Atelinae) - PGM11, ACP12, HBA2, HBB2 and ALB3.

S. f. weddelli (H = 4.1%) and S. midas midas (H = 5.6%) presented the highest H values, although in the case of the latter taxon, the small sample size (N = 13) may mean that this value is not representative of the levels of variability occurring in natural populations. The value of 5% for A. belzebul, the outgroup in the present study, was similar to that recorded for this species by Schneider et al. (1991). By contrast, the S. bicolor subspecies showed the lowest H values (Table VI), only slightly higher than those recorded for Leontopithecus rosalia (H = 0.7%; Forman et al., 1986) and Cebus apella paraguayanus (H = 1.2%; Sampaio et al., 1991). The matrix of genetic distances (Table VII) also shows that S. b. bicolor and S.b. martinsi are the most closely related, and in accordance with these values, we suggest that they represent a single taxon, S. bicolor.

The genetic distance recorded between S. midas midas and S. midas niger (D = 0.05) is well within the threshold of 0.15 defined by Thorpe (1982) for allopatric subspecies, and supports their classification as such. It is interesting to note, however, that the value of 0.07 recorded between S. midas midas and the S. bicolor populations also falls within this range, whereas those recorded between the latter and S. midas niger are of the order of 0.14, as might be expected from the geographic distribution of these populations. S. midas midas and S. bicolor are parapatric in the north of the Amazon, while S. midas niger occurs to the south of this river, some 500 km east of the eastern limit of the range of S. bicolor.

The UPGMA (Figure 1) and in particular the neighbor-joining (Figure 2 ) trees also reinforce the close ties between S. bicolor and S. midas populations, especially the parapatric populations. In addition to supporting the species-group arrangements of Natori and Hanihara (1992), Ferrari (1993), and Rylands et al. (1993), the observed values all point to the possibility that these populations represent subspecies of Saguinus midas Linnaeus, 1758, which, in accordance with the above observations on the status of the S. bicolor forms, would encompass a total of three subspecies, S. midas midas, S. midas bicolor and S. midas niger. If confirmed by additional data, this proposal would have significant implications for the conservation of the pied tamarins (bicolor forms), one of, if not the rarest and most endangered of Amazonian primates (Egler, 1993).

As expected, the analyses also supported relatively close ties between S. fuscicollis and S. mystax (Figures 1 and 2 ) which are clearly sister taxa as expected from their geographical and morphological proximity, although the distance values between them and the S. midas subspecies were also smaller than might be expected (Table VII), reflecting the genetic homogeneity of the callitrichines in general (Nagai et al., 1986; Melo et al., 1992; Dantas, 1994; Nagamachi, 1995; Meireles, C., Sampaio, I., Schneider, H., Ferrari, S.F., Coimbra-Filho, A.F., Pissinatti, A. and Schneider, M.P.C., unpublished results). Clearly, more data from a larger number of taxa will be needed before the taxonomic relationships within the genus can be defined with precision.

ACKNOWLEDGMENTS

We are grateful to Arlindo Pinto de Souza Junior for technical assistance and José Augusto Pereira Carneiro Muniz (Centro Nacional de Primatas) for supplying samples. Research supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP), Fundação de Amparo e Desenvolvimento da Pesquisa (FADESP), and Universidade Federal do Pará (UFPa).

RESUMO

A variabilidade genética de seis taxa de tamarins, gênero Saguinus, foi analisada comparativamente usando-se dados protéicos de onze sistemas codificados por quinze loci. S. fuscicollis weddelli e S. midas midas foram os taxa mais polimórficos, enquanto S. bicolor foi o menos. Os resultados da análise filogenética (UPGMA e neighbor-joining) e as distâncias genéticas entre os taxa foram em geral consistentes com suas relações geográficas e filogenéticas. As análises das populações de S. bicolor e S. midas indicaram que eles podem representar não mais do que três subespécies de uma única espécie, S. midas, com as formas de bicolor pertencendo a uma única subespécie, S. midas bicolor. Se apoiado por estudos adicionais, este fato teria implicações importantes para a conservação da forma de bicolor, que está em perigo de extinção. A similaridade genética de S. fuscicollis e S. mystax foi também consistente com sua proximidade geográfica e morfológica, embora mais dados sobre um número maior de taxa seriam necessários antes de se definirem as relações taxonômicas dentro do gênero.

REFERENCES

Coimbra-Filho, A.F. (1990). Sistemática, distribuição geográfica e situação atual dos símios brasileiros (Platyrrhini, Primates). Rev. Bras. Biol. 50: 1063-1079.

Dantas, S.M.M. (1994). Estudos citogenéticos em oito subespécies do gênero Saguinus (Primates). Master’s thesis, Universidade Federal do Pará, Belém, Brasil.

de Vivo, M. (1991). Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Fundação Biodiversitas, Belo Horizonte, Minas Gerais, Brasil, pp. 105.

Egler, S.G. (1993). First field study of the pied tamarin; Saguinus bicolor bicolor. Neotropical Primates 1: 13-14.

Ferrari, S.F. (1993). The adaptive radiation of Amazonian callitrichids (Primates, Platyrrhini). Evol. Biol. 7: 81-103.

Forman, L., Kleiman, D.G., Bush, R.M., Dietz, J.M., Ballou, J.D., Phillips, L.G., Coimbra-Filho, A.F. and O’Brien, S.J. (1986). Genetic variation within and among lion tamarins. Am. J. Phys. Anthropol. 71: 1-11.

Franco, M.H.L.P. and Salzano, F.M. (1985). A comparative study of albumin variants found in Brazil. Human Hered. 35: 34-38.

Hanihara, T. and Natori, M. (1987). Preliminary analysis for numerical taxonomy of the genus Saguinus based on dental measurements. Primates 28: 517-523.

Harris, H. and Hopkinson, D.A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics. North-Holland Publishing Company, Amsterdam.

Hershkovitz, P. (1977). Living New World Monkeys (Platyrrhini) with an Introduction to Primates. Vol. I. University of Chicago Press, Chicago.

Hershkovitz, P. (1979). Races of the emperor tamarin, Saguinus imperator Goeldi (Callitrichidae, Primates). Primates 20: 277-287.

Hershkovitz, P. (1982). Subspecies and geographic distribution of black-mantle tamarins Saguinus nigricollis Spix (Primates: Callitrichidae). Proc. Biol. Soc. Wash. 95: 647-656.

Hershkovitz, P. (1990). Titis, New World monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zool. 55: 1-109.

Kumar, S., Tamura, K. and Nei, M. (1993). MEGA - Molecular Evolutionary Analysis. Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park.

Melo, A.C.A., Sampaio, M.I.C., Schneider, M.P.C. and Schneider, H. (1992). Biochemical diversity and genetic distance in two species of the genus Saguinus. Primates 33: 217-225.

Mittermeier, R.A., Rylands, A.B. and Coimbra-Filho, A.F. (1988). Systematics: species and subspecies - an update. In: Ecology and Behavior of Neotropical Primates (Mittermeier, R.A., Rylands, A.B., Coimbra-Filho, A.F. and Fonseca, G.A.B., eds.). Vol. 2. World Wildlife Fund., Washington, D.C., pp. 13-75.

Mittermeier, R.A., Schwarz, M. and Ayres, J.M. (1992). A new species of marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates) from the Rio Maués region, State of Amazonas, central Brazilian Amazonia. Goeldiana Zoologia 14: 1-17.

Nagai, A., Shimaoka, T., Lee, S.C. and Ikemoto, S. (1986). Genetic markers in the blood of three species of tamarins (Saguinus mystax, S. labiatus and S. oedipus). Exp. Anim. 35: 375-380.

Nagamachi, C.Y. (1995). Relações cromossômicas e análises filogenética e de agrupamento na família Callitrichidae (Platyrrhini, Primates). Doctoral thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brasil.

Natori, M. and Hanihara, T. (1992). Variations in dental measurements between Saguinus species and their systematic relationships. Folia Primatol. 58: 84-92.

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.

Nei, M. (1987). Molecular Evolutionary Genetics. Columbia University Press, New York.

Reed, T.E. and Schull, W.J. (1968). A general maximum likelihood estimation program. Am. J. Hum. Genet. 20: 579-580.

Rylands, A.B., Coimbra-Filho, A.F. and Mittermeier, R.A. (1993). Systematics, geographic distribution, and some notes on the conservation status of the Callitrichidae. In: Marmosets and Tamarins: Systematics, Ecology, and Behaviour (Rylands, A.B., ed.). Oxford University Press, Oxford, pp. 11-77.

Saitou, N. and Nei, M. (1987). The neighbor-joining method; a new method for reconstructing phylogeneic trees. Mol. Biol. Evol. 4: 406-425.

Sampaio, M.I.C. and Schneider, M.P.C. (1986). Electrophoretic studies of a natural population of Chiropotes satanas (Cebidae, Platyrrhini) from the Amazonian region. Rev. Bras. Genet. 9: 67-74.

Sampaio, M.I.C., Schneider, M.P.C., Salzano, F.M. and Barroso, C.M.L. (1986). Esterase D and carbonic anhydrase 2 in a natural population of Cebus apella from Brazil. Primates 27: 363-367.

Sampaio, M.I.C., Barroso, C.M.L., Silva, B.T.F., Seuanez, H., Matayoshi, T., Howlin, E., Nazassi, N., Nagle, C. and Schneider, H. (1991). Genetic variability in Cebus apella paraguayanus: biochemical analysis of seven loci and variation in glyoxalase I (E.C. 4.4.1.5). Primates 32: 105-109.

Schneider, H., Sampaio, M.I.C., Schneider, M.P.C., Ayres, J.M., Barroso, C.M.L., Hamel, A., Silva, B.T.F. and Salzano, F.M. (1991). Coat color and biochemical variation in Amazonian wild population of Alouatta belzebul. Am. J. Phys. Anthropol. 85: 85-93.

Schneider, H., Schneider, M.P.C., Sampaio, I., Harada, M.L., Stanhope, M., Czelusniak, J. and Goodman, M. (1993). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol. Phylog. Evol. 2: 225-242.

Schneider, M.P.C. (1988). Variação protéica em primatas da Amazônia e seu significado evolutivo. Doctoral thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brasil.

Shows, T.B., Alper, C.A., Bootsma, D., Dorf, M., Douglas, T., Huisman, T., Kit, S., Klinger, H.P., Kozak, C., Lalley, P.A., Lindsley, D., Mcalpine, P.J., Mcdougall, J.K., Meera Khan, P., Meisler, M., Morton, N.E., Opitz, J.M., Partridge, C.W., Payne, R., Roderick, T.H., Rubinstein, P., Ruddle, F.H., Shaw, M., Spranger, J.W. and Weiss, K. (1979). International system for human gene nomenclature (ISGN). Cytogenet. Cell Genet. 25: 96-116.

Thorington Jr., R.W. (1988). Taxonomic status of Saguinus tripartitus (Milne-Edwards, 1878). Am. J. Primatol. 15: 367-371.

Thorpe, J.P. (1982). The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Ann. Rev. Ecol. Syst. 13: 139-168.

(Received June 10, 1996)

  • Coimbra-Filho, A.F. (1990). Sistemática, distribuição geográfica e situação atual dos símios brasileiros (Platyrrhini, Primates). Rev. Bras. Biol. 50: 1063-1079.
  • de Vivo, M. (1991). Taxonomia de Callithrix Erxleben, 1777 (Callitrichidae, Primates). Fundação Biodiversitas, Belo Horizonte, Minas Gerais, Brasil, pp. 105.
  • Egler, S.G. (1993). First field study of the pied tamarin; Saguinus bicolor bicolor Neotropical Primates 1: 13-14.
  • Ferrari, S.F. (1993). The adaptive radiation of Amazonian callitrichids (Primates, Platyrrhini). Evol. Biol. 7: 81-103.
  • Franco, M.H.L.P. and Salzano, F.M. (1985). A comparative study of albumin variants found in Brazil. Human Hered. 35: 34-38.
  • Hanihara, T. and Natori, M. (1987). Preliminary analysis for numerical taxonomy of the genus Saguinus based on dental measurements. Primates 28: 517-523.
  • Harris, H. and Hopkinson, D.A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics North-Holland Publishing Company, Amsterdam.
  • Hershkovitz, P. (1977). Living New World Monkeys (Platyrrhini) with an Introduction to Primates Vol. I. University of Chicago Press, Chicago.
  • Hershkovitz, P. (1979). Races of the emperor tamarin, Saguinus imperator Goeldi (Callitrichidae, Primates). Primates 20: 277-287.
  • Hershkovitz, P. (1982). Subspecies and geographic distribution of black-mantle tamarins Saguinus nigricollis Spix (Primates: Callitrichidae). Proc. Biol. Soc. Wash. 95: 647-656.
  • Hershkovitz, P. (1990). Titis, New World monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zool. 55: 1-109.
  • Kumar, S., Tamura, K. and Nei, M. (1993). MEGA - Molecular Evolutionary Analysis Institute of Molecular Evolutionary Genetics, Pennsylvania State University, University Park.
  • Melo, A.C.A., Sampaio, M.I.C., Schneider, M.P.C. and Schneider, H. (1992). Biochemical diversity and genetic distance in two species of the genus Saguinus. Primates 33: 217-225.
  • Mittermeier, R.A., Schwarz, M. and Ayres, J.M. (1992). A new species of marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates) from the Rio Maués region, State of Amazonas, central Brazilian Amazonia. Goeldiana Zoologia 14: 1-17.
  • Nagai, A., Shimaoka, T., Lee, S.C. and Ikemoto, S. (1986). Genetic markers in the blood of three species of tamarins (Saguinus mystax, S. labiatus and S. oedipus). Exp. Anim. 35: 375-380.
  • Nagamachi, C.Y. (1995). Relações cromossômicas e análises filogenética e de agrupamento na família Callitrichidae (Platyrrhini, Primates). Doctoral thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brasil.
  • Natori, M. and Hanihara, T. (1992). Variations in dental measurements between Saguinus species and their systematic relationships. Folia Primatol. 58: 84-92.
  • Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
  • Nei, M. (1987). Molecular Evolutionary Genetics Columbia University Press, New York.
  • Reed, T.E. and Schull, W.J. (1968). A general maximum likelihood estimation program. Am. J. Hum. Genet. 20: 579-580.
  • Saitou, N. and Nei, M. (1987). The neighbor-joining method; a new method for reconstructing phylogeneic trees. Mol. Biol. Evol. 4: 406-425.
  • Sampaio, M.I.C. and Schneider, M.P.C. (1986). Electrophoretic studies of a natural population of Chiropotes satanas (Cebidae, Platyrrhini) from the Amazonian region. Rev. Bras. Genet. 9: 67-74.
  • Sampaio, M.I.C., Schneider, M.P.C., Salzano, F.M. and Barroso, C.M.L. (1986). Esterase D and carbonic anhydrase 2 in a natural population of Cebus apella from Brazil. Primates 27: 363-367.
  • Sampaio, M.I.C., Barroso, C.M.L., Silva, B.T.F., Seuanez, H., Matayoshi, T., Howlin, E., Nazassi, N., Nagle, C. and Schneider, H. (1991). Genetic variability in Cebus apella paraguayanus: biochemical analysis of seven loci and variation in glyoxalase I (E.C. 4.4.1.5). Primates 32: 105-109.
  • Schneider, H., Sampaio, M.I.C., Schneider, M.P.C., Ayres, J.M., Barroso, C.M.L., Hamel, A., Silva, B.T.F. and Salzano, F.M. (1991). Coat color and biochemical variation in Amazonian wild population of Alouatta belzebul. Am. J. Phys. Anthropol. 85: 85-93.
  • Schneider, H., Schneider, M.P.C., Sampaio, I., Harada, M.L., Stanhope, M., Czelusniak, J. and Goodman, M. (1993). Molecular phylogeny of the New World monkeys (Platyrrhini, Primates). Mol. Phylog. Evol. 2: 225-242.
  • Schneider, M.P.C. (1988). Variação protéica em primatas da Amazônia e seu significado evolutivo. Doctoral thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Brasil.
  • Shows, T.B., Alper, C.A., Bootsma, D., Dorf, M., Douglas, T., Huisman, T., Kit, S., Klinger, H.P., Kozak, C., Lalley, P.A., Lindsley, D., Mcalpine, P.J., Mcdougall, J.K., Meera Khan, P., Meisler, M., Morton, N.E., Opitz, J.M., Partridge, C.W., Payne, R., Roderick, T.H., Rubinstein, P., Ruddle, F.H., Shaw, M., Spranger, J.W. and Weiss, K. (1979). International system for human gene nomenclature (ISGN). Cytogenet. Cell Genet. 25: 96-116.
  • Thorington Jr., R.W. (1988). Taxonomic status of Saguinus tripartitus (Milne-Edwards, 1878). Am. J. Primatol. 15: 367-371.
  • Thorpe, J.P. (1982). The molecular clock hypothesis: biochemical evolution, genetic differentiation and systematics. Ann. Rev. Ecol. Syst. 13: 139-168.

Publication Dates

  • Publication in this collection
    13 Oct 1998
  • Date of issue
    Mar 1997

History

  • Received
    10 June 1996
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